Microtubules are polarised α/β-tubulin-based polymers essential for cell viability, providing pushing and pulling forces, structural support or tracks for the transport of intracellular cargo (Goodson and Jonasson, 2018). α-tubulin is located at the so-called minus end and β-tubulin is exposed at the so-called plus end, which is typically more dynamic. This inherent microtubule polarity is important for cell polarity, as different motor proteins (Kinesins and Dynein) move cargo along microtubules in a specific direction – Dynein towards the minus end and most Kinesins towards the plus end. In neurons, most plus ends point away from the soma in axons (plus-end-out microtubules), while the microtubules in dendrites are either of mixed polarity or are predominantly minus-end-out (Hill et al., 2012; Kapitein and Hoogenraad, 2015; Kelliher et al., 2019; Tas et al., 2017). This difference between axons and dendrites is important for the correct distribution of cargo throughout the neuron (Harterink et al., 2018; Kapitein and Hoogenraad, 2015; Tas et al., 2017).

Within cells de novo assembly of new microtubules, that is microtubule nucleation, is kinetically unfavourable and is templated and catalysed by multi-protein γ-tubulin ring complexes (γ-TuRCs) (Tovey and Conduit, 2018). Knockdown of γ-TuRCs within model systems affects dynamic microtubules in all neuronal compartments (Nguyen et al., 2014; Ori-McKenney et al., 2012; Sánchez-Huertas et al., 2016; Yamada and Hayashi, 2019; Yau et al., 2014) and mutations in γ-TuRC genes have been linked to human neurodevelopmental disorders (Bahi-Buisson et al., 2014; Mitani et al., 2019; Poirier et al., 2013). γ-TuRCs are typically inactive until they are recruited to specific sites within cells, such as microtubule organising centres (MTOCs), the cytosol around mitotic chromatin, or the sides of pre-existing microtubules via binding to Augmin/HAUS complexes (Farache et al., 2018; Lin et al., 2015; Meunier and Vernos, 2016; Sanchez and Feldman, 2017; Teixido-Travesa et al., 2012). A range of MTOCs exist, including centrosomes, the Golgi apparatus and the nuclear envelope, and different cells use different MTOCs to help generate and organise their specific microtubule arrays (Sanchez and Feldman, 2017). γ-TuRC recruitment occurs via γ-TuRC ‘tethering proteins’, such as Drosophila Centrosomin (Cnn), that simultaneously bind to the γ-TuRC and a particular MTOC, and can also help activate the γ-TuRC (Tovey and Conduit, 2018).

Although γ-tubulin is important within neurons (Nguyen et al., 2014; Ori-McKenney et al., 2012; Sánchez-Huertas et al., 2016; Yamada and Hayashi, 2019; Yau et al., 2014), it remains unclear how microtubule nucleation is regulated. During early development of mammalian neurons, the centrosome within the soma nucleates microtubules (Stiess et al., 2010) that are severed and transported into neurites via motor-based microtubule sliding (Baas et al., 2005). Microtubule sliding is also important for axon outgrowth in Drosophila cultured neurons (Del Castillo et al., 2015; Lu et al., 2013), and for establishing microtubule polarity (del Castillo et al., 2015; Klinman et al., 2017; Rao et al., 2017; Yan et al., 2013; Zheng et al., 2008). Centrosomes are inactivated, however, at later developmental stages (Stiess et al., 2010) and are dispensable for neuronal development in both mammalian and fly neurons (Nguyen et al., 2011; Stiess et al., 2010). No other active MTOCs within the neuronal soma have been described. Nevertheless, microtubules continue to grow within the soma (Nguyen et al., 2011; Sánchez-Huertas et al., 2016), and in mammalian neurons this depends in part on the HAUS complex (Sánchez-Huertas et al., 2016), which is also important for microtubule growth within axons and dendrites (Cunha-Ferreira et al., 2018; Sánchez-Huertas et al., 2016). Some MTOCs have been identified within dendrites: the basal body, or its surrounding region, within the distal part of C. elegans ciliated neurons acts as an MTOC, as does a similar region within the URX non-ciliated neuron (Harterink et al., 2018); an MTOC made from endosomes that tracks the dendritic growth cone in C. elegans PVD neurons has recently been identified (Liang et al., 2020); and fragments of Golgi called Golgi outposts within the dendrites of Drosophila dendritic arborisation (da) neurons are thought to recruit γ-TuRCs and act as MTOCs (Ori-McKenney et al., 2012; Yalgin et al., 2015; Zhou et al., 2014).

Drosophila larval da neurons are a popular in vivo neuronal model (Jan and Jan, 2010). Ease of imaging and genetic manipulation coupled with the ability to examine different neuronal classes, each with a stereotypical dendritic branching pattern, make them a model of choice when examining microtubule organisation within neurons. Four classes exist, including class I neurons that are proprioceptive and have the simplest ‘comb-like’ dendritic branching pattern, and class IV neurons that are nociceptive and have the most elaborate branching pattern, tiling the surface of the larva (Figure 1—figure supplement 1; Grueber et al., 2002). In both neuronal classes, microtubules in axons are predominantly plus-end-out throughout development, but microtubule polarity in dendrites progressively becomes more minus-end-out as the neurons develop; at two days post larval hatching the majority of dynamic microtubules are minus-end-out (Hill et al., 2012; Stone et al., 2008). Microtubule polarity within da neurons can be disrupted when microtubule regulators are depleted (Mattie et al., 2010; Nguyen et al., 2014; Ori-McKenney et al., 2012; Rolls and Jegla, 2015; Sears and Broihier, 2016; Weiner et al., 2016; Yalgin et al., 2015; Zhou et al., 2014), but we lack a full understanding of how microtubule polarity is established and maintained.

Golgi outposts are thought to provide localised sites of microtubule nucleation within the dendrites of da neurons to help regulate dendritic outgrowth and microtubule polarity (Ori-McKenney et al., 2012; Yalgin et al., 2015; Zhou et al., 2014). Unlike the somatic Golgi, which comprises cis, medial, and trans compartments organised into stacks and ribbons (Kondylis and Rabouille, 2009; Nakamura et al., 1995), Golgi outposts can be either single- or multi-compartment units with multi-compartment units having a higher propensity to initiate microtubule growth (Zhou et al., 2014). Within class I da neurons, Golgi outpost-mediated nucleation is thought to be dependent on the γ-TuRC-tethering protein Cnn and to help restrict dendritic branching (Yalgin et al., 2015), while within class IV neurons Golgi outpost-mediated nucleation is believed to be dependent on Pericentrin-like protein (Plp) and to help promote dendritic branching (Ori-McKenney et al., 2012). There remains some uncertainty, however, about the role of Golgi outposts in microtubule nucleation, as a separate study that examined the localisation of ectopically expressed γ-tubulin-GFP concluded that γ-tubulin localises predominantly to dendritic branch points in a Golgi outpost-independent manner (Nguyen et al., 2014).

In this study, we initially aimed to identify sites of microtubule nucleation within Drosophila da neurons. We used endogenously tagged γ-tubulin-GFP as a proxy for γ-TuRCs and performed a detailed analysis of γ-tubulin localisation within both class I and class IV da neurons. We find variation between neuronal classes in how γ-tubulin localises within dendrites, but find that the most prominent localisation of γ-tubulin is at the cis-compartment of somatic Golgi stacks within all sensory neurons of the dorsal cluster. This asymmetric γ-tubulin-Golgi association is not dependent on either Cnn or Plp, suggesting another molecule must regulate γ-TuRC recruitment to the Golgi. Tracking of EB1-GFP comets within the soma suggests that microtubules are nucleated asymmetrically from the somatic Golgi. We find that these Golgi-derived microtubules initially grow preferentially towards the axon. During growth, they are also guided towards the axon and away from dendrites in a Kinesin-2-dependent manner, and they readily enter the axon contributing to plus-end-out microtubule polarity. In contrast, the relatively small number of microtubules that do grow towards a dendrite are normally excluded and this also depends upon Kinesin-2. After Kinesin-2 depletion, growing microtubules more readily approach and enter the dendrites causing a dramatic increase in the proportion of anterograde microtubules in proximal dendrites. This results in a reversal of overall microtubule polarity in proximal dendrites from predominantly minus-end-out to predominantly plus-end-out. We therefore propose that plus-end-associated Kinesin-2 guides growing microtubules towards the axon and away from dendrites along a polarised microtubule network within the soma, while at dendrite entry points Kinesin-2 generates a stalling force on growing microtubules when engaging dendritic microtubules of opposite polarity.

Understanding of how neuronal microtubules are generated and organised is a matter of much interest and importance. In this paper, we have used Drosophila da neurons as an in vivo model system to address these questions. Our results have led us to propose a model that describes how microtubules are generated and organised within the soma, which also impacts the microtubule populations within proximal axons and dendrites. This model comprises multiple elements. Firstly, the model states that microtubules are nucleated asymmetrically from the somatic Golgi, growing initially with a preference towards the axon and away from dendrites. Secondly, plus-end-associated Kinesin-2 helps guide these growing microtubules towards the axon and away from dendrites along a polarised network of microtubules within the soma. Thirdly, plus-end-associated Kinesin-2 also helps prevent any microtubules that do approach the entrance to a dendrite from entering. We propose that a combination of these mechanisms is essential to maintain minus-end-out polarity in proximal dendrites, a key feature that distinguishes dendrites from axons.

We have shown that endogenously tagged γ-tubulin23C-GFP, which is a proxy for the major catalysts of microtubule nucleation, γ-TuRCs, localises predominantly to the Golgi stacks within the soma of da neurons, and to a few Golgi outposts within the proximal branches of class IV da neurons. Our data show that the ability of γ-tubulin to localise to these Golgi structures does not depend upon either Cnn or Plp, both of which have been implicated in recruiting γ-TuRCs to Golgi outposts within dendrites of class I and class IV da neurons, respectively (Ori-McKenney et al., 2012; Yalgin et al., 2015). Thus, γ-tubulin, presumably in the form of γ-TuRCs, must be recruited to the Golgi by another tethering protein, perhaps by one of the large coiled-coil ‘Golgin’ proteins that project from specific parts of the Golgi (Munro, 2011).

After showing that γ-tubulin-GFP localised to the somatic Golgi, we tracked EB1-GFP comets from the Golgi and found that they grew with an initial directional preference towards the axon, suggestive of asymmetric nucleation. This analysis was more robust under normal conditions than after cooling-warming cycles, because more comets could be analysed (it was difficult to keep the imaging plane consistent during temperature shifting, due to temperature-induced glass expansion/contraction). Thus, while an equal number of Golgi-derived comets (4) grew towards and away from the axon after warming in Figure 6—Video 2, we believe this perceived lack of asymmetry is most likely due to chance, especially as a fraction of comets can grow in more random directions even under normal conditions (Figure 6C). We therefore propose that there is a genuine preference for growth of Golgi-derived microtubules towards the axon. This may be explained, at least in part, by the asymmetric localisation of γ-tubulin at the somatic Golgi stacks. Using markers of cis- and trans-Golgi, we have found that γ-tubulin localises preferentially to the cis-Golgi. This is also true in mammalian cells, where the somatic Golgi acts as an asymmetric MTOC in various cell types, such as migrating fibroblasts and different types of cultured mammalian cells in interphase (Rios, 2014). It has been proposed that asymmetric microtubule nucleation is due to the presence of CLASP proteins at the trans-Golgi, which have been suggested to bind and stabilise the plus ends of microtubules that are nucleated by γ-TuRCs at the cis-Golgi (Vinogradova et al., 2009). Whether this occurs in Drosophila neurons remains to be explored. Drosophila CLASP is known to be a plus-tip protein within axons (Beaven et al., 2015) and is required for axon guidance (Lee et al., 2004), but to our knowledge a role for CLASP at the Golgi in any Drosophila cell type has not yet been reported. In mammalian cells, directional microtubule nucleation is thought to be important for cell motility in fibroblasts (Efimov et al., 2007) and for polarised pseudopod formation during invasion of cancer cells (Wu et al., 2016). Our data suggest that asymmetric nucleation at the somatic Golgi in Drosophila da neurons may establish a polarised microtubule network within the soma and is important for ensuring that plus-end-out microtubules enter axons rather than dendrites.

It is possible that a fraction of comets that originate from the somatic Golgi represent microtubules that were re-growing after partial depolymerisation, where the re-growth event happened to overlap a Golgi stack. However, several pieces of evidence suggest that the majority of the Golgi-derived comets represent nucleation events. First, γ-tubulin accumulates strongly at the somatic Golgi and a high accumulation of γ-TuRCs at a particular site is normally indicative of a nucleation site, such as when γ-TuRCs accumulate at mitotic centrosomes. Second, we have found that comets emerge repeatedly from the Golgi in a similar direction, strongly suggestive of repeated nucleation events. Third, we believe it is unlikely that all of the comets emerging from the Golgi after a cooling-warming cycle represent microtubules that had not fully depolymerised and that just happened to re-grow close to the Golgi. Moreover, comets that emerged from the Golgi a significant amount of time after warming did not emerge in the same direction as those that had grown immediately after warming. This strongly suggests they are not the same microtubule re-growing after depolymerisation but represent new nucleation events. Direct imaging of microtubules could help assess the degree of overall microtubule depolymerisation induced by cooling, although cold-resistant microtubules that may remain after cooling could impede the ability to visualise depolymerisation of dynamic microtubules, especially if the dynamic microtubules had originally grown alongside the stable microtubules. Increasing the cooling time before inducing regrowth may cause the depolymerisation of all microtubules, and this could be tested by using fluorescent markers of microtubules or by fixing and immunostaining the samples. These experiments have limitations, however, as keeping the animal alive for long enough to depolymerise all microtubule may be challenging and fixing and staining experiments do not allow one to observe the same neuron before, during, and after cooling. In summary, when we consider all of our data as a whole, we believe the most parsimonious conclusion is that microtubules are nucleated asymmetrically from the somatic Golgi.

It has previously been shown that centrosomes in Drosophila neurons do not act as MTOCs (Nguyen et al., 2011), and our observations that EB1-GFP comets do not emerge radially from a single source support this conclusion. In other cell types the somatic Golgi can ‘compete’ with centrosomes for the ability to organise microtubules, where decreasing nucleation from one organelle increases nucleation at the other (Gavilan et al., 2018; Ríos et al., 2004; Wu et al., 2016). It is therefore possible that the lack of microtubule nucleation at centrosomes in Drosophila neurons enables microtubules to be nucleated at the Golgi. In mammalian neurons the centrosome is deactivated after the first few days in culture (Stiess et al., 2010). An intriguing possibility is that this deactivation allows the Golgi to organise microtubules, which may be necessary to ensure correct microtubule polarity during later neuronal development, although nucleation from the Golgi in mammalian neurons has yet to be reported.

Our analysis was carried out in third instar larvae where the neurons are fully developed and functional. Axons have already extended and made connections in the central nervous system and dendritic arbors are largely established. It is thus somewhat surprising that microtubules continue to be nucleated within the soma. It is possible that somatic microtubules are necessary for transport of cargos to axonal and dendritic entry sites. Given that Golgi-derived microtubules grow preferentially towards the axon and that somatic Golgi stacks are distributed throughout the soma, there is likely an overall microtubule polarity within the soma itself, with more plus ends pointing towards the axon. Even small biases in the orientation of microtubules within a network can be important for the polarised distribution of components, such as in Drosophila oocytes (Zimyanin et al., 2008). A similar bias within neuronal soma could be important for directing molecules into axons and dendrites. Perhaps this asymmetric microtubule network within the soma, as well as the microtubules within the axon, need constant renewal. There is evidence that molecular motors can damage microtubules (Triclin et al., 2018) and so the large amount of motor-driven transport that occurs within neurons may necessitate microtubule renewal from the soma.

A key feature of our model is the action of plus-end-associated Kinesin-2. Our Kap3 RNAi data suggest that Kinesin-2 is required to guide growing microtubules along a polarised microtubule network within the soma towards the axon and away from dendrites, although future experiments with dual-colour imaging of microtubules and EB1-GFP comets will help support this conclusion. Our data also suggest that plus-end-associated Kinesin-2 prevents outward growing plus ends of somatic microtubules from entering dendrites. Within the soma, we envisage that when a somatic microtubule approaches another somatic microtubule at an acute angle (<90°), it can readily turn and be guided along that microtubule (Figure 8A,C). Kinesin-2 mediated "collision resolution" events occur at dendritic branch points in class I da neurons to ensure growing microtubules turn towards the soma (Weiner et al., 2016) and turning events have been recapitulated in vitro (Chen et al., 2014; Doodhi et al., 2014). One study showed that the in vitro turning events also occured at obtuse angles (>90°), where the growing microtubule buckled to allow the plus end to remain in contact with the ‘rail’ microtubule. This could presumably also occur within the soma of da neurons. The frequency of guidance events, however, decreases significantly as the angle increases (Doodhi et al., 2014). In contrast to the microtubule collision events that will occur with variable angles within the neuronal soma, when outward growing somatic microtubules try to grow into a dendrite they will always encounter dendritic microtubules at angles close to 180° (Figure 8B,C), because most dendritic microtubules are oriented minus-end-out and also because of the limited space available at dendrite entry points. Kinesin-2 motors on the plus end of the outward growing somatic microtubules could engage with the shafts of the minus-end-out dendritic microtubules and generate a backwards force when attempting to ‘walk’ towards the plus end of the dendritic microtubule i.e. in a direction opposite to which the plus end of the somatic microtubule is attempting to grow. This backward force would presumably lead to stalling of the plus end and thus depolymerisation of the microtubule. It is also possible that Kinesin-2 motors slide the plus end along the dendritic microtubule back into the soma, but this sliding action requires the growing microtubule to buckle and thus requires sufficient space (Doodhi et al., 2014). Thus, buckling may be impeded at the narrow dendrite entry site anddepolymerisation favoured. Kinesin-2 motors should be sufficient to induce stalling of microtubule growth, because growing microtubules generate a force of ~3–4 pN (Dogterom and Yurke, 1997), while a single Kinesin-2 motor generates a force of ~5 pN (Schroeder et al., 2012). Depolymerisation upon stalling could be equivalent to how depolymerisation is induced when microtubules grow against immovable objects (Janson et al., 2003). Importantly, this model elegantly explains why microtubules from the soma are prevented from growing into the dendrites while dendritic microtubules can readily grow into the soma. Other models, such as if a high concentration of a microtubule depolymerase was present at dendritic entry sites, could not distinguish between these two events. In contrast, our model predicts that dendritic microtubules can grow readily into the soma because they do not frequently encounter a microtubule with opposite polarity, except for the occasional somatic microtubule attempting to grow into a dendrite.

Our model explains how minus-end-out microtubule polarity is maintained within proximal dendrites, but what is the origin of minus-end-out microtubules? These microtubules could have been pushed out from the soma minus end first by motor-based sliding, a mechanism known to promote initial axon outgrowth in cultured Drosophila neurons (Lu et al., 2013; Lu et al., 2015). Alternatively, or in conjunction with this, they could have been nucleated at sites within dendrites and then have grown back towards the soma. Retrograde microtubule growth events do occur within the dendrites of da neurons, and some of these growth events originate from Golgi outposts (Ori-McKenney et al., 2012; Yalgin et al., 2015; Zhou et al., 2014) and from early endosomes at branchpoints (Weiner et al., 2020). It was shown that γ-tubulin co-localises with early endosome markers at class I branchpoints and that this localisation relies on Wnt signalling proteins (Weiner et al., 2020). Our observation that endogenously-tagged γ-tubulin localises to branchpoints supports this conclusion. Moreover, it was recently shown that an endosome-based MTOC tracks the growing dendritic growth cone within C. elegans PVD neurons and nucleates microtubules that travel back towards the soma (Liang et al., 2020). The authors also suggest that a similar process may occur in newly developing Drosophila class I neurons. We also observe γ-tubulin within dendritic bubbles and dendritic stretches, but whether γ-tubulin is also recruited to these regions by endosomes, or by cytosolic accumulations of γ-TuRC tethering proteins such as Cnn or Plp, will need to be addressed in future studies. While our data suggest that γ-TuRCs are absent from the majority of Golgi outposts, they appear to be present at a few proximal Golgi outposts within class IV neurons. Moreover, microtubule growth events from Golgi outposts could be independent of γ-TuRCs; other non-γ-TuRC microtubule binding proteins can promote microtubule nucleation in vitro (Roostalu and Surrey, 2017), and ectopic Golgi outposts within the axons of nudE mutants promote microtubule growth but not via γ-TuRCs (Arthur et al., 2015; Yang and Wildonger, 2020). Thus, there are several potential mechanisms to generate minus-end-out microtubules within dendrites, that will need to be explored further in future.

It will be interesting in future to examine whether the plus ends of somatic microtubules can grow into dendrites more readily during early neuronal development, when there may be fewer minus-end-out microtubules within dendrites. If true, there must come a developmental point at which the balance shifts and microtubules are prevented from growing into dendrites. This shift could occur in several different ways, including upregulating the number of retrograde microtubules nucleated within dendrites, upregulating Kinesin-2, or changing the direction of microtubule nucleation within the soma. These are all interesting possibilities that are now open for investigation in the future.

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 6 and 7.

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Author details

1. Amrita Mukherjee

   Department of Zoology, University of Cambridge, Cambridge, United Kingdom

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

2. Paul S Brooks

   Department of Zoology, University of Cambridge, Cambridge, United Kingdom

   Contribution

   Resources, Data curation, Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

3. Fred Bernard

   Université de Paris, CNRS, Institut Jacques Monod, Paris, France

   Contribution

   Resources

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7919-253X

4. Antoine Guichet

   Université de Paris, CNRS, Institut Jacques Monod, Paris, France

   Contribution

   Resources, Data curation, Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7216-1944

5. Paul T Conduit

   1. Department of Zoology, University of Cambridge, Cambridge, United Kingdom
   2. Université de Paris, CNRS, Institut Jacques Monod, Paris, France

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   paul.conduit@ijm.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7822-1191

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